Skip to main content Accessibility help
×
Home

Response inhibition in alcohol-dependent patients and patients with depression/anxiety: a functional magnetic resonance imaging study

  • Z. Sjoerds (a1) (a2), W. van den Brink (a2), A. T. F. Beekman (a1), B. W. J. H. Penninx (a1) (a3) (a4) and D. J. Veltman (a1)...

Abstract

Background

The inability to inhibit certain behaviors is a key feature of impulsivity, which is often present in people with a substance use disorder. However, the findings on impulsivity in people with alcohol dependence (AD) are inconsistent, possibly because of the frequent co-occurrence of depression/anxiety (D/A) and its influence on impulsivity. In the current study, we aimed to distinguish response inhibition impairments in AD from possible response inhibition effects associated with D/A.

Method

AD patients (n = 31) with high D/A co-morbidity were compared to patients with D/A only (n = 18) and healthy controls (HCs; n = 16) using the Stop Signal Task (SST) during functional magnetic resonance imaging (fMRI). Correlation analyses were performed between activated brain areas, behavioral data and addiction and D/A characteristics.

Results

The three groups did not differ on response inhibition performance. However, AD severity, but not D/A severity, was positively associated with decreased response inhibition. During the SST, AD patients showed hyperactivity in the putamen and thalamus compared with D/A patients and HCs. Thalamus activation was negatively associated with AD duration. In addition, AD patients showed hypoactivity in the supplementary motor area (SMA) compared with HCs. SMA activity within HCs was negatively correlated with depressive symptom severity.

Discussion

In general, AD patients were not more impulsive than D/A patients or HCs but they did reveal inhibition impairments with increasing AD severity. A shift from cortical to subcortical engagement in AD patients during response inhibition may represent an alternative strategy, which decreased with longer drinking history, suggesting the presence of an AD-specific endophenotype.

Copyright

Corresponding author

* Address for correspondence: Z. Sjoerds, M.Sc., VU University Medical Center, Department of Psychiatry, Van der Boechorststraat 7, MF-A422, 1081 BT Amsterdam, The Netherlands. (Email: sjoerds.zs@gmail.com)

References

Hide All
Achenbach, TM (1966). The classification of children's psychiatric symptoms: a factor-analytic study. Psychological Monographs 80, 137.
Aron, AR (2011). From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biological Psychiatry 69, e55e68.
Aron, AR, Poldrack, RA (2006). Cortical and subcortical contributions to Stop signal response inhibition: role of the subthalamic nucleus. Journal of Neuroscience 26, 24242433.
Babor, TF, Hofmann, M, DelBoca, FK, Hesselbrock, V, Meyer, RE, Dolinsky, ZS, Rounsaville, B (1992). Types of alcoholics, I. Evidence for an empirically derived typology based on indicators of vulnerability and severity. Archives of General Psychiatry 49, 599608.
Babor, TF, Kranzler, HR, Lauerman, RJ (1989). Early detection of harmful alcohol consumption: comparison of clinical, laboratory, and self-report screening procedures. Addictive Behaviors 14, 139157.
Baler, RD, Volkow, ND (2006). Drug addiction: the neurobiology of disrupted self-control. Trends in Molecular Medicine 12, 559566.
Beck, AT, Epstein, N, Brown, G, Steer, RA (1988). An inventory for measuring clinical anxiety: psychometric properties. Journal of Consulting and Clinical Psychology 56, 893897.
Bellani, M, Hatch, JP, Nicoletti, MA, Ertola, AE, Zunta-Soares, G, Swann, AC, Brambilla, P, Soares, JC (2012). Does anxiety increase impulsivity in patients with bipolar disorder or major depressive disorder? Journal of Psychiatric Research 46, 616621.
Bobb, DS Jr., Adinoff, B, Laken, SJ, McClintock, SM, Rubia, K, Huang, HW, Husain, MM, Mapes, KS, Tamminga, C, Cullum, CM, Gopinath, K, Trivedi, MH, Kozel, FA (2012). Neural correlates of successful response inhibition in unmedicated patients with late-life depression. American Journal of Geriatric Psychiatry 20, 10571069.
Boschloo, L, Vogelzangs, N, Smit, JH, van den Brink, W, Veltman, DJ, Beekman, ATF, Penninx, BWJH (2011). Comorbidity and risk indicators for alcohol use disorders among persons with anxiety and/or depressive disorders. Findings from the Netherlands Study of Depression and Anxiety (NESDA). Journal of Affective Disorders 131, 233242.
Brett, M, Anton, J-L, Valabreque, R, Poline, J-B (2002). Region of interest analysis using an SPM toolbox [Abstract]. Presented at the 8th International Conference on Functional Mapping of the Human Brain, 2–6 June 2002, Sendai, Japan. Available on CD-ROM in Neuroimage 16, no. 2, Abstract 497 (http://matthew.dynevor.org/_downloads/marsbar_abstract.pdf)
Broos, N, Schmaal, L, Wiskerke, J, Kostelijk, L, Lam, T, Stoop, N, Weierink, L, Ham, J, de Geus, EJ, Schoffelmeer, AN, van den Brink, W, Veltman, DJ, de Vries, TJ, Pattij, T, Goudriaan, AE (2012). The relationship between impulsive choice and impulsive action: a cross-species translational study. PLoS One 7, e36781.
Cai, W, Leung, HC (2011). Rule-guided executive control of response inhibition: functional topography of the inferior frontal cortex. PLoS One 6, e20840.
Cloninger, CR, Bohman, M, Sigvardsson, S (1981). Inheritance of alcohol abuse. Cross-fostering analysis of adopted men. Archives of General Psychiatry 38, 861868.
de Graaf, R, Bijl, RV, Smit, F, Vollebergh, WAM, Spijker, J (2002). Risk factors for 12-month comorbidity of mood, anxiety, and substance use disorders: findings from the Netherlands Mental Health Survey and Incidence Study. American Journal of Psychiatry 159, 620629.
Deichmann, R, Gottfried, JA, Hutton, C, Turner, R (2003). Optimized EPI for fMRI studies of the orbitofrontal cortex. NeuroImage 19, 430441.
de Jong, R, Coles, MG, Logan, GD, Gratton, G (1990). In search of the point of no return: the control of response processes. Journal of Experimental Psychology. Human Perception and Performance 16, 164182.
de Ruiter, MB, Oosterlaan, J, Veltman, DJ, van den Brink, W, Goudriaan, AE (2012). Similar hyporesponsiveness of the dorsomedial prefrontal cortex in problem gamblers and heavy smokers during an inhibitory control task. Drug and Alcohol Dependence 121, 8189.
Diener, C, Kuehner, C, Brusniak, W, Ubl, B, Wessa, M, Flor, H (2012). A meta-analysis of neurofunctional imaging studies of emotion and cognition in major depression. NeuroImage 61, 677685.
Dom, G, D'haene, P, Hulstijn, W, Sabbe, B (2006). Impulsivity in abstinent early- and late-onset alcoholics: differences in self-report measures and a discounting task. Addiction 101, 5059.
Etkin, A, Prater, KE, Hoeft, F, Menon, V, Schatzberg, AF (2010). Failure of anterior cingulate activation and connectivity with the amygdala during implicit regulation of emotional processing in generalized anxiety disorder. American Journal of Psychiatry 167, 545554.
Eugene, F, Joormann, J, Cooney, RE, Atlas, LY, Gotlib, IH (2010). Neural correlates of inhibitory deficits in depression. Psychiatry Research 181, 3035.
Evenden, JL (1999). Varieties of impulsivity. Psychopharmacology 146, 348361.
Everitt, BJ, Belin, D, Economidou, D, Pelloux, Y, Dalley, JW, Robbins, TW (2008). Review. Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363, 31253135.
Everitt, BJ, Robbins, TW (2005). Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nature Neuroscience 8, 14811489.
Forman, SD, Dougherty, GG, Casey, BJ, Siegle, GJ, Braver, TS, Barch, DM, Stenger, VA, Wick-Hull, C, Pisarov, LA, Lorensen, E (2004). Opiate addicts lack error-dependent activation of rostral anterior cingulate. Biological Psychiatry 55, 531537.
Fox, PT, Lancaster, JL (1994). Neuroscience on the net. Science 266, 994996.
Friston, KJ, Holmes, AP, Poline, JB, Grasby, PJ, Williams, SC, Frackowiak, RS, Turner, R (1995). Analysis of fMRI time-series revisited. NeuroImage 2, 4553.
Fu, LP, Bi, GH, Zou, ZT, Wang, Y, Ye, EM, Ma, L, Ming, Fan, Yang, Z (2008). Impaired response inhibition function in abstinent heroin dependents: an fMRI study. Neuroscience Letters 438, 322326.
Goldstein, RZ, Volkow, ND (2002). Drug addiction and its underlying neurobiological basis: neuroimaging evidence for the involvement of the frontal cortex. American Journal of Psychiatry 159, 16421652.
Gray, JA, McNaughton, N (2000). The Neuropsychology of Anxiety, An Enquiry into the Function of the Septo-Hippocampal System. Oxford University Press: New York.
Heatherton, TF, Kozlowski, LT, Frecker, RC, Fagerstrom, KO (1991). The Fagerstrom Test for Nicotine Dependence: a revision of the Fagerstrom Tolerance Questionnaire. British Journal of Addiction 86, 11191127.
Heslenfeld, DJ, Oosterlaan, J (2003). Where does the brain stop? Brain areas involved in the inhibition of behavior. Journal of Psychophysiology 17, 138.
Hester, R, Garavan, H (2004). Executive dysfunction in cocaine addiction: evidence for discordant frontal, cingulate, and cerebellar activity. Journal of Neuroscience 24, 1101711022.
Hur, JW, Kim, YK (2009). Comparison of clinical features and personality dimensions between patients with major depressive disorder and normal control. Psychiatry Investigation 6, 150155.
Jakubczyk, A, Klimkiewicz, A, Topolewska-Wochowska, A, Serafin, P, Sadowska-Mazuryk, J, Pupek-Pyziol, J, Brower, KJ, Wojnar, M (2012). Relationships of impulsiveness and depressive symptoms in alcohol dependence. Journal of Affective Disorders 136, 841847.
Jentsch, JD, Taylor, JR (1999). Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Psychopharmacology 146, 373390.
Joormann, J, Dkane, M, Gotlib, IH (2006). Adaptive and maladaptive components of rumination? Diagnostic specificity and relation to depressive biases. Behavior Therapy 37, 269280.
Joormann, J, Gotlib, IH (2010). Emotion regulation in depression: relation to cognitive inhibition. Cognition and Emotion 24, 281298.
Karch, S, Jager, L, Karamatskos, E, Graz, C, Stammel, A, Flatz, W, Lutz, J, Holtschmidt-Taschner, B, Genius, J, Leicht, G, Pogarell, O, Born, C, Moller, HJ, Hegerl, U, Reiser, M, Soyka, M, Mulert, C (2008). Influence of trait anxiety on inhibitory control in alcohol-dependent patients: simultaneous acquisition of ERPs and BOLD responses. Journal of Psychiatric Research 42, 734745.
Katz, R, De Sanctis, P, Mahoney, JR, Sehatpour, P, Murphy, CF, Gomez-Ramirez, M, Alexopoulos, GS, Foxe, JJ (2010). Cognitive control in late-life depression: response inhibition deficits and dysfunction of the anterior cingulate cortex. American Journal of Geriatric Psychiatry 18, 10171025.
Kaufman, JN, Ross, TJ, Stein, EA, Garavan, H (2003). Cingulate hypoactivity in cocaine users during a GO-NOGO task as revealed by event-related functional magnetic resonance imaging. Journal of Neuroscience 23, 78397843.
Kirby, KN, Petry, NM (2004). Heroin and cocaine abusers have higher discount rates for delayed rewards than alcoholics or non-drug-using controls. Addiction 99, 461471.
Krueger, RF (1999). The structure of common mental disorders. Archives of General Psychiatry 56, 921926.
Lambert, C, Zrinzo, L, Nagy, Z, Lutti, A, Hariz, M, Foltynie, T, Draganski, B, Ashburner, J, Frackowiak, R (2012). Confirmation of functional zones within the human subthalamic nucleus: patterns of connectivity and sub-parcellation using diffusion weighted imaging. NeuroImage 60, 8394.
Lau, MA, Christensen, BK, Hawley, LL, Gemar, MS, Segal, ZV (2007). Inhibitory deficits for negative information in persons with major depressive disorder. Psychological Medicine 37, 12491259.
Lawrence, AJ, Luty, J, Bogdan, NA, Sahakian, BJ, Clark, L (2009). Impulsivity and response inhibition in alcohol dependence and problem gambling. Psychopharmacology 207, 163172.
Li, CS, Huang, C, Constable, RT, Sinha, R (2006). Imaging response inhibition in a stop-signal task: neural correlates independent of signal monitoring and post-response processing. Journal of Neuroscience 26, 186192.
Li, CS, Huang, C, Yan, P, Bhagwagar, Z, Milivojevic, V, Sinha, R (2008 a). Neural correlates of impulse control during stop signal inhibition in cocaine-dependent men. Neuropsychopharmacology 33, 17981806.
Li, CS, Luo, X, Yan, P, Bergquist, K, Sinha, R (2009). Altered impulse control in alcohol dependence: neural measures of stop signal performance. Alcoholism: Clinical and Experimental Research 33, 740750.
Li, CS, Yan, P, Sinha, R, Lee, TW (2008 b). Subcortical processes of motor response inhibition during a stop signal task. NeuroImage 41, 13521363.
Liddle, PF, Kiehl, KA, Smith, AM (2001). Event-related fMRI study of response inhibition. Human Brain Mapping 12, 100109.
Lipszyc, J, Schachar, R (2010). Inhibitory control and psychopathology: a meta-analysis of studies using the stop signal task. Journal of the International Neuropsychological Society: JINS 16, 10641076.
Logan, GD (1994). On the ability to inhibit thought and action: a user's guide to the stop signal paradigm. In Inhibitory Processes in Attention, Memory and Language (ed. Dagenbach, D. and Carr, T. H.), pp. 189239. Academic Press: San Diego, CA.
Lubman, DI, Yucel, M, Pantelis, C (2004). Addiction, a condition of compulsive behaviour? Neuroimaging and neuropsychological evidence of inhibitory dysregulation. Addiction 99, 14911502.
Maldjian, JA, Laurienti, PJ, Kraft, RA, Burdette, JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 19, 12331239.
Matthews, S, Simmons, A, Strigo, I, Gianaros, P, Yang, T, Paulus, M (2009). Inhibition-related activity in subgenual cingulate is associated with symptom severity in major depression. Psychiatry Research 172, 16.
Nambu, A, Tokuno, H, Takada, M (2002). Functional significance of the cortico-subthalamo-pallidal ‘hyperdirect’ pathway. Neuroscience Research 43, 111117.
Ngo, HTT, Street, HL, Hulse, GK (2011). Is there a relationship between impulsivity and depression in adults? A research synthesis. Current Psychiatry Reviews 7, 281297.
Nielsen, FA, Hansen, LK (2002). Automatic anatomical labeling of Talairach coordinates and generation of volumes of interest via the BrainMap database. Neuroimage 16(2). Available on CD-ROM (http://www2.imm.dtu.dk/pubdb/views/publication_details.php?id=195). Presented at the 8th International Conference on Functional Mapping of the Human Brain, 2–6 June 2002, Sendai, Japan.
Noel, X, Van der Linden, M, Brevers, D, Campanella, S, Verbanck, P, Hanak, C, Kornreich, C, Verbruggen, F (2012). Separating intentional inhibition of prepotent responses and resistance to proactive interference in alcohol-dependent individuals. Drug and Alcohol Dependence 128, 200205.
Patton, JH, Stanford, MS, Barratt, ES (1995). Factor structure of the Barratt Impulsiveness Scale. Journal of Clinical Psychology 51, 768774.
Peluso, MAM, Hatch, JP, Glahn, DC, Monkul, ES, Sanches, M, Najt, P, Bowden, CL, Barratt, ES, Soares, JC (2007). Trait impulsivity in patients with mood disorders. Journal of Affective Disorders 100, 227231.
Penninx, BWJH, Beekman, ATF, Smit, JH, Zitman, FG, Nolen, WA, Spinhoven, P, Cuijpers, P, de Jong, PJ, van Marwijk, HWJ, Assendelft, WJJ, van der Meer, K, Verhaak, P, Wensing, M, de Graaf, R, Hoogendijk, WJ, Ormel, J, van Dyck, R (2008). The Netherlands Study of Depression and Anxiety (NESDA): rationale, objectives and methods. International Journal of Methods in Psychiatric Research 17, 121140.
Perry, JL, Carroll, ME (2008). The role of impulsive behavior in drug abuse. Psychopharmacology 200, 126.
Robins, LN, Wing, J, Wittchen, HU, Helzer, JE, Babor, TF, Burke, J, Farmer, A, Jablenski, A, Pickens, R, Regier, DA, Sartorius, N, Towle, LH (1988). The Composite International Diagnostic Interview. An epidemiologic instrument suitable for use in conjunction with different diagnostic systems and in different cultures. Archives of General Psychiatry 45, 10691077.
Robinson, TE, Berridge, KC (2003). Addiction. Annual Review of Psychology 54, 2553.
Rubia, K, Smith, AB, Brammer, MJ, Taylor, E (2003). Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection. NeuroImage 20, 351358.
Rush, AJ, Gullion, CM, Basco, MR, Jarrett, RB, Trivedi, MH (1996). The Inventory of Depressive Symptomatology (IDS): psychometric properties. Psychological Medicine 26, 477486.
Schmaal, L, Joos, L, Koeleman, M, Veltman, DJ, van den Brink, W, Goudriaan, AE (2012). Effects of modafinil on neural correlates of response inhibition in alcohol-dependent patients. Biological Psychiatry 73, 211218.
Spielberger, CD, Gorsuch, RL, Lushene, RE (1970). STAI Manual for the State-Trait Anxiety Inventory. Consulting Psychologists Press: Palo Alto, CA.
Sullivan, JT, Sykora, K, Schneiderman, J, Naranjo, CA, Sellers, EM (1989). Assessment of alcohol withdrawal: the revised clinical institute withdrawal assessment for alcohol scale (CIWA-Ar). British Journal of Addiction 84, 13531357.
Tricomi, E, Balleine, BW, O'Doherty, JP (2009). A specific role for posterior dorsolateral striatum in human habit learning. European Journal of Neuroscience 29, 22252232.
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, Mazoyer, B, Joliot, M (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15, 273289.
Vandermeeren, R, Hebbrecht, M (2012). The dual process model of addiction. Towards an integrated model? [in Dutch] Tijdschrift voor Psychiatrie 54, 731740.
van Holst, RJ, Schilt, T (2011). Drug-related decrease in neuropsychological functions of abstinent drug users. Current Drug Abuse Reviews 4, 4256.
van Strien, JW (1992). Classification of left- and right-handed research participants [in Dutch]. Nederlands Tijdschrift voor de Psychologie 47, 8892.
Worsley, KJ, Marrett, S, Neelin, P, Vandal, AC, Friston, KJ, Evans, AC (1996). A unified statistical approach for determining significant signals in images of cerebral activation. Human Brain Mapping 4, 5873.
Yang, TT, Simmons, AN, Matthews, SC, Tapert, SF, Frank, GK, Bischoff-Grethe, A, Lansing, AE, Wu, J, Brown, GG, Paulus, MP (2009). Depressed adolescents demonstrate greater subgenual anterior cingulate activity. Neuroreport 20, 440444.
Zandbelt, BB, Vink, M (2010). On the role of the striatum in response inhibition. PLoS One 5, e13848.

Keywords

Type Description Title
PDF
Supplementary materials

Sjoerds Supplementary Material
Supplementary Methods

 PDF (292 KB)
292 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed